Complex Sexually Dimorphic Traits

Spanke et al. BMC Ecol Evo (2021) 21:57 BMC Ecology and Evolution https://doi.org/10.1186/s12862-021-01791-z RESEARCH ARTICLE Open Access Complex sexually dimorphic traits shape the parallel evolution of a novel reproductive strategy in Sulawesi ricefshes (Adrianichthyidae) Tobias Spanke1, Leon Hilgers1, Benjamin Wipfer1, Jana M. Flury1, Arne W. Nolte2, Ilham V. Utama3, Bernhard Misof1, Fabian Herder1 and Julia Schwarzer1* Abstract Background: Pelvic brooding is a form of uni-parental care, and likely evolved in parallel in two lineages of Sulawesi ricefshes. Contrary to all other ricefshes, females of pelvic brooding species do not deposit eggs at a substrate (transfer brooding), but carry them until the fry hatches. We assume that modifcations reducing the costs of egg carrying are benefcial for pelvic brooding females, but likely disadvantageous in conspecifc males, which might be resolved by the evolution of sexual dimorphism via sexual antagonistic selection. Thus we hypothesize that the evolution of pelvic brooding gave rise to female-specifc skeletal adaptations that are shared by both pelvic brooding lineages, but are absent in conspecifc males and transfer brooding species. To tackle this, we combine 3D-imaging and morphometrics to analyze skeletal adaptations to pelvic brooding. Results: The morphology of skeletal traits correlated with sex and brooding strategy across seven ricefsh species. Pelvic brooding females have short ribs caudal of the pelvic girdle forming a ventral concavity and clearly elongated and thickened pelvic fns compared to both sexes of transfer brooding species. The ventral concavity limits the body cavity volume in female pelvic brooders. Thus body volumes are smaller compared to males in pelvic brooding species, a pattern sharply contrasted by transfer brooding species. Conclusions: We showed in a comparative framework that highly similar, sexually dimorphic traits evolved in parallel in both lineages of pelvic brooding ricefsh species. Key traits, present in all pelvic brooding females, were absent or much less pronounced in conspecifc males and both sexes of transfer brooding species, indicating that they are non- benefcial or even maladaptive for ricefshes not providing extended care. We assume that the combination of ventral concavity and robust, elongated fns reduces drag of brooding females and provides protection and stability to the egg cluster. Thus ricefshes are one of the rare examples where environmental factors rather than sexual selection shaped the evolution of sexually dimorphic skeletal adaptations. Keywords: Maternal care, Ribs, Rib length, Sexual dimorphism, Sexual antagonistic selection, Oryzias, Adrianichthys Background Examples of repeated parallel or convergent evolution *Correspondence: [email protected] are omnipresent, i.e. the evolution of similar phenotypes 1 Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee shaped by the same selective regimes that may or may 160, 53113 Bonn, Germany Full list of author information is available at the end of the article not trace back to a common ancestor [1–3]. Prominent © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. 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BMC Ecol Evo (2021) 21:57 Page 2 of 16 examples in the animal kingdom are fight, advanced brooding was suggested to have evolved as adaptation eyes [4], or the evolution of parental care, from the most to the absence of suitable spawning substrates in pelagic common state of no-care to extended care [5], like pla- habitats [24]. Some morphological adaptations to pelvic cental viviparity [6]. In species that conduct care, selec- brooding, namely elongated pelvic fns (frst described by tive burden is often unevenly distributed among the sexes [31] and [32]) and the presence of a ventral concavity in and impacts sex specifc life histories. In organisms with females [28], are well known (see also [23, 24, 27, 29]). As uni-parental care, costs of care only arise for one par- few studies have performed comparative analyses among ent so selection to increase individual ftness can difer Oryzias species, data remained mostly descriptive, lack- extremely between the sexes [7–9]. Te resulting sexual ing information on sexual dimorphism (e.g. in A. oopho- confict can be resolved by sex specifc adaptations to rus) and have no statistical support (but see [24]). In most parental care [10]. Nonetheless, only a few cases of sex- transfer brooding ricefsh species, sex-specifc diferences ually dimorphic traits are known that are not primarily in pelvic fn length were not described. Recent studies, shaped by sexual selection, but instead evolved as a trade- however, reported sex-specifc diferences in pelvic fn of between ecological constraints and adaptation to uni- length in the newly described transfer brooding species parental care [11–15]. External bearing [16, 17] or egg Oryzias soerotoi and O. dopingdopingensis [33, 34], indi- brooding [18] is a form of parental care in which eggs are cating the need for more detailed analyses. carried externally, attached to the parents body, some- In the present study, we build upon prior knowledge times by specialized structures, or in the parents mouth. and place it in a comparative framework of seven species, In some of these cases, eggs are nurtured [19] by either of representing all phylogenetic lineages within the endemic the parents. Compared with egg attendance, where par- ricefshes from Sulawesi ([22], Fig. 1). To gain a more ents remain with the eggs at a fxed location, egg brood- conclusive picture regarding sex specifc diferences and ing is particularly advantageous in variable environments skeletal adaptations to pelvic brooding, we used high- [18], as brooding parents can move freely to escape egg- resolution µ-computed tomography (µ-CT) imaging and predation and unfavorable habitat conditions. Carrying morphometrics and focus on adaptations of the ribs and the brood may however require anatomical adaptations, pelvic fns. We further investigated, how changes in body which can include the evolution of highly specialized tis- shape in pelvic brooding females, i.e. the presence of the sues and organs, like brood pouches and incubating areas ventral concavity, afected the volume of their body cav- in seahorses and pipefshes [20, 21]. ity. We hypothesized that pelvic brooding females have In Sulawesi ricefshes (Beloniformes, Adrianichthyidae) a reduced body cavity volume, when compared to con- a specifc form of external bearing called ‘pelvic brood- specifc males or transfer brooding species. Since pelvic ing’ evolved from ancestral transfer brooding between 16 brooding is a form of uni-parental care, only the care- and 3 mya in large lacustrine Adrianichthys species [22] giver bears potential costs of egg carrying. Such costs and about 1–1.5 mya within one lineage of closely related can be higher energetic demands [35, 36] or an increased Oryzias species [22–24]. Most ricefshes are transfer predation risk of the care-giver [26]. We thus assume, brooders, which means that females carry a clutch of fer- that modifcations reducing the costs of egg carrying are tilized eggs via attaching flaments that protrude from benefcial for pelvic brooding females, but disadvanta- their urogenital pore. Te eggs are deposited a few hours geous in conspecifc males. Te resulting sexual confict after mating [25, 26]. In contrast, females of pelvic brood- could be resolved by the evolution of sexual dimorphism ing species carry their eggs until the fry hatches; for up via sexual antagonistic selection. Hence, we hypothesized to 18 days after spawning [27]. Female pelvic brood- that the evolution of pelvic brooding gave rise to female- ers situate the egg cluster in a ventral concavity, while specifc skeletal adaptations that are shared between both using their conspicuously elongated pelvic fns to cover pelvic brooding lineages, but are absent in conspecifc the eggs (Fig. 1) [24, 28, 29]. Additionally, female pelvic males and transfer brooding species. brooders slow down oocyte maturation [27] and form a tissue that anchors the eggs’ attaching flaments inside Results the ovarian cavity [29]. Tis illustrates that the evolu- Specifc ribs are shorter in females of pelvic brooding tion of pelvic brooding from transfer brooding likely ricefshes entails a set of physiological and anatomical adaptations. Intersexual diferences in rib length were present in Details on most of these aspects, however, remain scarce pelvic brooding ricefsh species (O. eversi, O. sarasino- and current knowledge on both transfer brooding and rum and A. oophorus) and interspecifc diferences were pelvic brooding is based mainly on single species stud- present between females of pelvic brooding and trans- ies (e.g. [24, 25, 27, 30]). Although ecological data on fer brooding (O. celebensis, O. nigrimas, O. wolasi, O. this exceptional reproductive strategy is limited, pelvic matanensis) ricefshes (Figs. 2, 3). Spanke et al. BMC Ecol Evo (2021) 21:57 Page 3 of 16 Fig. 1 Study system: the endemic ricefshes of Sulawesi. a Simplifed ricefsh phylogeny with emphasis on Sulawesi ricefshes.

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